Persistent legacy effects on soil metagenomes facilitate plant adaptive responses to drought

Both chronic and acute drought alter the composition and physiology of soil microbiota by selecting for functional traits that preserve fitness in dry conditions. Currently, little is known about how the resulting precipitation legacy effects manifest at the molecular and physiological levels and how they influence neighboring plants, especially in the context of subsequent drought. We characterized metagenomes of six prairie soils spanning a steep precipitation gradient in Kansas, USA. By statistically controlling for variation in soil porosity and elemental profiles, we identified bacterial taxa and functional gene categories associated with precipitation. This microbial precipitation legacy persisted through a 5-month-long experimental drought and mitigated the negative physiological effects of acute drought for a wild grass species that is native to the precipitation gradient, but not for the domesticated crop species maize. In particular, microbiota with a low-precipitation legacy altered transcription of a subset of host genes that mediate transpiration and intrinsic water use efficiency during drought. Our results show how long-term exposure to water stress alters soil microbial communities with consequences for the drought responses of neighboring plants.